Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
Identifieur interne : 000238 ( Pmc/Checkpoint ); précédent : 000237; suivant : 000239Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production
Auteurs : Andrew C. Doxey [Canada] ; Daniel A. Kurtz [Canada] ; Michael Dj Lynch [Canada] ; Laura A. Sauder [Canada] ; Josh D. Neufeld [Canada]Source :
- The ISME Journal [ 1751-7362 ] ; 2014.
Abstract
Cobalamin (vitamin B12) is a complex metabolite and essential cofactor required by many branches of life, including most eukaryotic phytoplankton. Algae and other cobalamin auxotrophs rely on environmental cobalamin supplied from a relatively small set of cobalamin-producing prokaryotic taxa. Although several
Url:
DOI: 10.1038/ismej.2014.142
PubMed: 25126756
PubMed Central: 4303638
Affiliations:
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<author><name sortKey="Kurtz, Daniel A" sort="Kurtz, Daniel A" uniqKey="Kurtz D" first="Daniel A" last="Kurtz">Daniel A. Kurtz</name>
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<author><name sortKey="Lynch, Michael Dj" sort="Lynch, Michael Dj" uniqKey="Lynch M" first="Michael Dj" last="Lynch">Michael Dj Lynch</name>
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<author><name sortKey="Sauder, Laura A" sort="Sauder, Laura A" uniqKey="Sauder L" first="Laura A" last="Sauder">Laura A. Sauder</name>
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<country xml:lang="fr">Canada</country>
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<author><name sortKey="Neufeld, Josh D" sort="Neufeld, Josh D" uniqKey="Neufeld J" first="Josh D" last="Neufeld">Josh D. Neufeld</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Biology, University of Waterloo</institution>
, Waterloo, Ontario,<country>Canada</country>
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<country xml:lang="fr">Canada</country>
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<idno type="doi">10.1038/ismej.2014.142</idno>
<date when="2014">2014</date>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Aquatic metagenomes implicate <italic>Thaumarchaeota</italic>
in global cobalamin production</title>
<author><name sortKey="Doxey, Andrew C" sort="Doxey, Andrew C" uniqKey="Doxey A" first="Andrew C" last="Doxey">Andrew C. Doxey</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Biology, University of Waterloo</institution>
, Waterloo, Ontario,<country>Canada</country>
</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Kurtz, Daniel A" sort="Kurtz, Daniel A" uniqKey="Kurtz D" first="Daniel A" last="Kurtz">Daniel A. Kurtz</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Biology, University of Waterloo</institution>
, Waterloo, Ontario,<country>Canada</country>
</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Lynch, Michael Dj" sort="Lynch, Michael Dj" uniqKey="Lynch M" first="Michael Dj" last="Lynch">Michael Dj Lynch</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Biology, University of Waterloo</institution>
, Waterloo, Ontario,<country>Canada</country>
</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Sauder, Laura A" sort="Sauder, Laura A" uniqKey="Sauder L" first="Laura A" last="Sauder">Laura A. Sauder</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Biology, University of Waterloo</institution>
, Waterloo, Ontario,<country>Canada</country>
</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Neufeld, Josh D" sort="Neufeld, Josh D" uniqKey="Neufeld J" first="Josh D" last="Neufeld">Josh D. Neufeld</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Biology, University of Waterloo</institution>
, Waterloo, Ontario,<country>Canada</country>
</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<series><title level="j">The ISME Journal</title>
<idno type="ISSN">1751-7362</idno>
<idno type="eISSN">1751-7370</idno>
<imprint><date when="2014">2014</date>
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<front><div type="abstract" xml:lang="en"><p>Cobalamin (vitamin B<sub>12</sub>
) is a complex metabolite and essential cofactor required by many branches of life, including most eukaryotic phytoplankton. Algae and other cobalamin auxotrophs rely on environmental cobalamin supplied from a relatively small set of cobalamin-producing prokaryotic taxa. Although several <italic>Bacteria</italic>
have been implicated in cobalamin biosynthesis and associated with algal symbiosis, the involvement of <italic>Archaea</italic>
in cobalamin production is poorly understood, especially with respect to the <italic>Thaumarchaeota</italic>
. Based on the detection of cobalamin synthesis genes in available thaumarchaeotal genomes, we hypothesized that <italic>Thaumarchaeota</italic>
, which are ubiquitous and abundant in aquatic environments, have an important role in cobalamin biosynthesis within global aquatic ecosystems. To test this hypothesis, we examined cobalamin synthesis genes across sequenced thaumarchaeotal genomes and 430 metagenomes from a diverse range of marine, freshwater and hypersaline environments. Our analysis demonstrates that all available thaumarchaeotal genomes possess cobalamin synthesis genes, predominantly from the anaerobic pathway, suggesting widespread genetic capacity for cobalamin synthesis. Furthermore, although bacterial cobalamin genes dominated most surface marine metagenomes, thaumarchaeotal cobalamin genes dominated metagenomes from polar marine environments, increased with depth in marine water columns, and displayed seasonality, with increased winter abundance observed in time-series datasets (e.g., L4 surface water in the English Channel). Our results also suggest niche partitioning between thaumarchaeotal and cyanobacterial ribosomal and cobalamin synthesis genes across all metagenomic datasets analyzed. These results provide strong evidence for specific biogeographical distributions of thaumarchaeotal cobalamin genes, expanding our understanding of the global biogeochemical roles played by <italic>Thaumarchaeota</italic>
in aquatic environments.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">ISME J</journal-id>
<journal-id journal-id-type="iso-abbrev">ISME J</journal-id>
<journal-title-group><journal-title>The ISME Journal</journal-title>
</journal-title-group>
<issn pub-type="ppub">1751-7362</issn>
<issn pub-type="epub">1751-7370</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25126756</article-id>
<article-id pub-id-type="pmc">4303638</article-id>
<article-id pub-id-type="pii">ismej2014142</article-id>
<article-id pub-id-type="doi">10.1038/ismej.2014.142</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Aquatic metagenomes implicate <italic>Thaumarchaeota</italic>
in global cobalamin production</article-title>
<alt-title alt-title-type="running"><italic>Thaumarchaeota</italic>
are global cobalamin producers</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Doxey</surname>
<given-names>Andrew C</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kurtz</surname>
<given-names>Daniel A</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lynch</surname>
<given-names>Michael DJ</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sauder</surname>
<given-names>Laura A</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Neufeld</surname>
<given-names>Josh D</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>Department of Biology, University of Waterloo</institution>
, Waterloo, Ontario,<country>Canada</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Department of Biology, University of Waterloo</institution>
, 200 University Avenue West, Waterloo, Ontario, <country>Canada</country>
N2L 3G1. E-mail: <email>acdoxey@uwaterloo.ca</email>
or <email>jneufeld@uwaterloo.ca</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>02</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub"><day>15</day>
<month>08</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>2</month>
<year>2015</year>
</pub-date>
<volume>9</volume>
<issue>2</issue>
<fpage>461</fpage>
<lpage>471</lpage>
<history><date date-type="received"><day>02</day>
<month>05</month>
<year>2014</year>
</date>
<date date-type="rev-recd"><day>02</day>
<month>07</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>03</day>
<month>07</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015 International Society for Microbial Ecology</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>International Society for Microbial Ecology</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 3.0 Unported License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0/">http://creativecommons.org/licenses/by/3.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>Cobalamin (vitamin B<sub>12</sub>
) is a complex metabolite and essential cofactor required by many branches of life, including most eukaryotic phytoplankton. Algae and other cobalamin auxotrophs rely on environmental cobalamin supplied from a relatively small set of cobalamin-producing prokaryotic taxa. Although several <italic>Bacteria</italic>
have been implicated in cobalamin biosynthesis and associated with algal symbiosis, the involvement of <italic>Archaea</italic>
in cobalamin production is poorly understood, especially with respect to the <italic>Thaumarchaeota</italic>
. Based on the detection of cobalamin synthesis genes in available thaumarchaeotal genomes, we hypothesized that <italic>Thaumarchaeota</italic>
, which are ubiquitous and abundant in aquatic environments, have an important role in cobalamin biosynthesis within global aquatic ecosystems. To test this hypothesis, we examined cobalamin synthesis genes across sequenced thaumarchaeotal genomes and 430 metagenomes from a diverse range of marine, freshwater and hypersaline environments. Our analysis demonstrates that all available thaumarchaeotal genomes possess cobalamin synthesis genes, predominantly from the anaerobic pathway, suggesting widespread genetic capacity for cobalamin synthesis. Furthermore, although bacterial cobalamin genes dominated most surface marine metagenomes, thaumarchaeotal cobalamin genes dominated metagenomes from polar marine environments, increased with depth in marine water columns, and displayed seasonality, with increased winter abundance observed in time-series datasets (e.g., L4 surface water in the English Channel). Our results also suggest niche partitioning between thaumarchaeotal and cyanobacterial ribosomal and cobalamin synthesis genes across all metagenomic datasets analyzed. These results provide strong evidence for specific biogeographical distributions of thaumarchaeotal cobalamin genes, expanding our understanding of the global biogeochemical roles played by <italic>Thaumarchaeota</italic>
in aquatic environments.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>Identification of the cobalamin synthesis pathway and associated gene clusters in available thaumarchaeotal genomes. The pathway in (<bold>a</bold>
) is adapted from the studies by <xref ref-type="bibr" rid="bib36">Moore <italic>et al.</italic>
(2013)</xref>
and <xref ref-type="bibr" rid="bib46">Raux <italic>et al.</italic>
(1999)</xref>
. Horizontal arrows indicate homology between aerobic and anaerobic pathway enzymes. Grey enzyme names were not detected in thaumarchaeotal genomes. *CbiJ is also not present in other known archaeal cobalamin producers and therefore should not be considered an essential gene for this pathway in <italic>Thaumarchaeota</italic>
. (<bold>b</bold>
) A six-member cobalamin synthesis gene cluster with conserved synteny across several thaumarchaeotal genomes. The cluster encodes enzymes (highlighted by blue boxes in (<bold>a</bold>
)) in the upper pathway, and includes three enzymes (bolded) specific to the anaerobic pathway. (<bold>c</bold>
) A four-member gene cluster possessing enzymes (highlighted by green boxes in (<bold>a</bold>
)) corresponding to the final steps of cobalamin synthesis. The apparent missing <italic>cobD</italic>
gene in AR1 may be a genome annotation error given that it appears to be in the genome but may be truncated (data not shown).</p>
</caption>
<graphic xlink:href="ismej2014142f1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>Survey of cobalamin synthesis genes across aquatic metagenomes. (<bold>a</bold>
) The full set of <italic>cob/cbi</italic>
genes and subset of eleven representative marker genes (black) used in the screen and their abundance (total number of detected genes). (<bold>b</bold>
) Taxonomic breakdown of all detected <italic>cob/cbi</italic>
genes across 430 aquatic metagenomes. (<bold>c</bold>
) Distributions of thaumarchaeotal, cyanobacterial and proteobacterial cobalamin gene contributions (% of total <italic>cob/cbi</italic>
genes) for 28 different studies. (<bold>d</bold>
) Clustering and heatmap visualization of taxonomic composition of <italic>cob/cbi</italic>
genes for the 430 metagenomes. The color scale reflects the proportion of <italic>cob/cbi</italic>
genes in each sample affiliated with a particular taxonomic group. More information on each sample can be found in <xref ref-type="supplementary-material" rid="sup1">Supplementary Table S1</xref>
. (<bold>e</bold>
) Global distribution of cobalamin synthesis genes. To emphasize <italic>Thaumarchaeota</italic>
-rich metagenomes, data points with higher thaumarchaeotal contributions have been slightly enlarged and overlayed preferentially in cases where there are overlapping data points. The <italic>Thaumarchaeota</italic>
-rich Arctic metagenome described in the text is indicated by an asterisk.</p>
</caption>
<graphic xlink:href="ismej2014142f2"></graphic>
</fig>
<fig id="fig3"><label>Figure 3</label>
<caption><p>Phylum and metadata correlations. (<bold>a</bold>
) Correlation matrix for all species-metadata correlations with <italic>r</italic>
>0.25. Correlations were measured between numerical metadata from all 430 metagenome samples and the per-taxon proportion of cobalamin genes. Correlations between taxonomic proportions were also measured to identify potential species–species associations. (<bold>b</bold>
) Left: proportion of cobalamin synthesis genes vs depth for three phyla (computed using all 430 metagenome samples). Middle: proportion of cobalamin synthesis genes vs different time points from the 2008–2009 L4 station time series. Right: per-gene taxonomic proportions of cobalamin genes for an Arctic metagenome. <italic>Thaumarchaeota</italic>
(red), <italic>Cyanobacteria</italic>
(green), <italic>Proteobacteria</italic>
(blue), Unclassified (dark grey), <italic>Bacteroidetes/Chlorobi</italic>
(purple), <italic>Actinobacteria</italic>
(black), <italic>Firmicutes</italic>
(orange), and Other (light gray). Bar widths are proportional to the square root of the sample sizes. (<bold>c</bold>
) Phyla-vs-Phyla contributions of cobalamin synthesis genes across all 430 metagenome samples. All correlations exhibit a negative linear relationship, except for <italic>Thaumarchaeota</italic>
-vs-<italic>Cyanobacteria</italic>
, which exhibits an either-or relationship, suggestive of competitive or niche exclusion. (<bold>d</bold>
) Correlation analysis for the MI_LOCO metagenome. The strongest correlating variables with thaumarchaeotal <italic>cob/cbi</italic>
gene contribution are shown on the left, and plots for the top two positively (nitrate concentration and sample depth) and negatively correlated (ammonium and bacterial cell concentration) variables are shown on the right.</p>
</caption>
<graphic xlink:href="ismej2014142f3"></graphic>
</fig>
<table-wrap id="tbl1"><label>Table 1</label>
<caption><title>The 15 most abundant species contributing detected metagenomic <italic>cob/cbi</italic>
genes across all datasets</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="left"></col>
<col align="char" char="."></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><italic>Species</italic>
</th>
<th align="left" valign="top" charoff="50"><italic>Phylum/class</italic>
</th>
<th align="char" valign="top" char="." charoff="50"><italic>cob/cbi genes</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50"><italic>Rhodobacterales</italic>
bacterium HTCC2255</td>
<td align="left" valign="top" charoff="50"><italic>Alphaproteobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">9091</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><bold><italic>Candidatus</italic>
Nitrosopumilus sp. AR2</bold>
</td>
<td align="left" valign="top" charoff="50"><italic>Thaumarchaeota</italic>
</td>
<td align="char" valign="top" char="." charoff="50">4394</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic><bold>Candidatus</bold>
</italic>
<bold>Nitrosopumilus salaria</bold>
</td>
<td align="left" valign="top" charoff="50"><italic>Thaumarchaeota</italic>
</td>
<td align="char" valign="top" char="." charoff="50">4110</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic><bold>Candidatus</bold>
</italic>
<bold>Nitrosoarchaeum limnia</bold>
</td>
<td align="left" valign="top" charoff="50"><italic>Thaumarchaeota</italic>
</td>
<td align="char" valign="top" char="." charoff="50">3656</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>SAR324 cluster bacterium</italic>
SCGC AAA001 C10</td>
<td align="left" valign="top" charoff="50"><italic>Alphaproteobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">3283</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic><bold>Nitrosopumilus maritimus</bold>
</italic>
<bold>SCM1</bold>
</td>
<td align="left" valign="top" charoff="50"><italic>Thaumarchaeota</italic>
</td>
<td align="char" valign="top" char="." charoff="50">2672</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>Prochlorococcus marinus</italic>
str. MIT 9301</td>
<td align="left" valign="top" charoff="50"><italic>Cyanobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">2422</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>Prochlorococcus marinus</italic>
str. AS9601</td>
<td align="left" valign="top" charoff="50"><italic>Cyanobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">2371</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>Gamma proteobacterium</italic>
SCGC AAA007 O20</td>
<td align="left" valign="top" charoff="50"><italic>Gammaproteobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">2279</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><bold><italic>Candidatus</italic>
Nitrosopumilus koreensis AR1</bold>
</td>
<td align="left" valign="top" charoff="50"><italic>Thaumarchaeota</italic>
</td>
<td align="char" valign="top" char="." charoff="50">2039</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>Chlorobium phaeovibrioides</italic>
DSM 265</td>
<td align="left" valign="top" charoff="50"><italic>Chlorobi</italic>
</td>
<td align="char" valign="top" char="." charoff="50">1942</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic><bold>Candidatus</bold>
</italic>
<bold>Nitrosoarchaeum koreensis</bold>
<bold>MY1</bold>
</td>
<td align="left" valign="top" charoff="50"><italic>Thaumarchaeota</italic>
</td>
<td align="char" valign="top" char="." charoff="50">1912</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>Neptuniibacter caesariensis</italic>
</td>
<td align="left" valign="top" charoff="50"><italic>Gammaproteobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">1663</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Endosymbiont of <italic>Bathymodiolus</italic>
sp.</td>
<td align="left" valign="top" charoff="50"><italic>Gammaproteobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">1571</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>Prochlorococcus marinus</italic>
subsp. <italic>pastoris</italic>
str. CCMP1986</td>
<td align="left" valign="top" charoff="50"><italic>Cyanobacteria</italic>
</td>
<td align="char" valign="top" char="." charoff="50">1226</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t1-fn1"><p>Taxonomic annotations were assigned based on the top BLAST match and are therefore dependent on the existing species diversity of the reference (NCBI) database. Thaumarchaeotal species are in bold.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>Canada</li>
</country>
</list>
<tree><country name="Canada"><noRegion><name sortKey="Doxey, Andrew C" sort="Doxey, Andrew C" uniqKey="Doxey A" first="Andrew C" last="Doxey">Andrew C. Doxey</name>
</noRegion>
<name sortKey="Kurtz, Daniel A" sort="Kurtz, Daniel A" uniqKey="Kurtz D" first="Daniel A" last="Kurtz">Daniel A. Kurtz</name>
<name sortKey="Lynch, Michael Dj" sort="Lynch, Michael Dj" uniqKey="Lynch M" first="Michael Dj" last="Lynch">Michael Dj Lynch</name>
<name sortKey="Neufeld, Josh D" sort="Neufeld, Josh D" uniqKey="Neufeld J" first="Josh D" last="Neufeld">Josh D. Neufeld</name>
<name sortKey="Sauder, Laura A" sort="Sauder, Laura A" uniqKey="Sauder L" first="Laura A" last="Sauder">Laura A. Sauder</name>
</country>
</tree>
</affiliations>
</record>
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